Surgical Classification of Endometriosis

Editorial Surgical Classi fication of Endometriosis João Nogueira Neto 1 Mauricio Simões Abrão 2,3 Eduardo Schor 4 Julio Cesar Rosa-e-Silva 5 1 Department of Gynecology and Obstetrics, Faculdade de Medicina, Universidade Federal do Maranhão, São Luis, MA, Brazil 2 Department of Gynecology, Bene ficência Portuguesa de São Paulo, São Paulo, SP , Brazil 3 Department of Gynecology and Obstetrics, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brazil 4 Department of Gynecology, Escola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, SP, Brazil 5 Department of Gynecology and Obstetrics, Faculdade de Medicina, Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP , Brazil Rev Bras Ginecol Obstet 2022;44(8):737 –739. Endometriosis is a chronic, benign, estrogen-dependent and multifactorial gynecological disease that mainly affects women of reproductive age. It can be de fined by the presence of tissue that resembles the endometrial gland and/or stroma outside the uterus, predominantly although not exclusively, in the female pelvis. 1 It is estimated that 10% of women of reproductive age have this disease, which represents around 176 million women worldwide, generat- ing direct costs to health systems and indirect costs due to reduced productivity, in addition to physical and psycho- logical suffering secondary to pain and infertility, with consequent loss of quality of life. 2 Given the many difficulties imposed by endometriosis, it has been extensively researched in recent decades.3,4 Its classifica- tion is one of the dif ficulties faced. A reproducible, easy-to- apply, and well-organized classification system is needed not only to clarify communication between clinicians, but also to standardize the optimal treatment strategy and clinical trials.2,5 The National Specialized Commission on Endometriosis of the Brazilian Federation of Gynecology and Obstetrics Asso- ciations – FEBRASGO analyzed the different forms of classi- fication chosen by the World Endometriosis Society (WES) 5 with the objective to standardize the current classi fication nationwide for Brazilian services that diagnose and treat this disease. As a single classi fication that evaluates all possible man- ifestations of endometriosis is lacking, four classi fications were standardized, among which: the revised classi fication of the American Society for Reproductive Medicine (rASRM), the ENZIAN classi fication, the Endometriosis Fertility Index (EFI) and the American Association of Gynecologic Laparos- copists (AAGL) classi fication. 2,6–10 The World Endometriosis Society (WES) published the first international consensus on the classi fication of endo- metriosis using a rigorous methodology in 2017. 5 The lack of a classi fication comprising all aspects of this disease led to the proposal of a combination of the most relevant classi- fications that could be used by all professionals working with women with endometriosis, from which surgeons can select the appropriate components and ensure its documentation in patients ’ records.5 The initial ASRM Classi fication proposed a single ap- proach in 1979. 6 The endometriosis stage is derived from a cumulative score according to the location and size of lesions observed during surgery. 2,6 The staging system underwent modifications in 1996 and is currently divided into I (1-5 points, minimal), II (6-15 points, mild), III (16-40 points, moderate) and IV (greater than 40 points, severe). The advantages of this classi fication are its global accep- tance, being widely used, easy application and the fact of helping patients to easily understand the stage of their disease. 2 Among the disadvantages are differences between histo- logically diagnosed endometriosis and the stage made by visualization, its low reproducibility, low correlation be- tween symptoms and its staging, not assessing the severity of pain and infertility, and not considering the presence of deep in filtrating endometriosis in areas such as uterosacral ligaments, bladder, vagina and intestine. 2,6,11,12 The ENZIAN classi fication was introduced in 2005 to determine the extent of deep endometriosis during surgical treatment, complementing the rASRM classi fication. This classification was already revised in 2010 and 2011 to correct its overlap with the rASRM and make it easier to use. 2,7 In Address for correspondence João Nogueira Neto, MD, Praça Gonçalves Dias, 65020-240, C e n t r o ,S ã oL u í s ,M A ,B r a z i l (e-mail: [email protected]). DOI https://doi.org/ 10.1055/s-0042-1755588. ISSN 0100-7203. © 2022. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/) Thieme Revinter Publicações Ltda., Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil THIEME Editorial 737 Article published online: 2022-09-08 2021, it was revised again to introduce the evaluation of the forms of peritoneal and ovarian endometriosis, and the assessment of tubal permeability through chromotubation and secondary adhesions. 13 This last review aimed to pro- pose a logical anatomical classi fication for use by a non- invasive method (magnetic resonance imaging and pelvic ultrasound), preoperatively, enabling a more adequate sur- gical planning, and intraoperatively, allowing a consistent and clear classification of deep endometriosis. Future studies are needed to assess its clinical validity, accuracy and reproducibility. 2,13 The advantages are that it describes the retroperitoneal structures, can be determined by imaging modality and used for surgical planning, and the location and extent of the disease are associated with the presence and severity of different symptoms such as pain. 2,5,14 The following are among the disadvantages: low level of global acceptance due to its complexity; patients ’ difficulty in understanding the classi fication informed given the com- plexity of stages and insuf ficient knowledge of pelvic anato- my by lay people; the classi fication will be imprecise if the surgical approach to deep lesions is performed incompletely or if the imaging study is not con firmed in the surgical procedure; and finally, even if the classi fication is previously made by imaging modality, there is still no scienti fic evi- dence on the usefulness of the classi fication determined by image, although it has great future potential because of the increasing percentage of patients in clinical follow-up of the disease.2 Another existing classi fication, the EFI, aims to develop a Fertility Index in patients with endometriosis, and predict the rate of spontaneous pregnancy in patients with endome- triosis undergoing surgical treatment who will not attempt to conceive with assisted reproduction techniques. 8 The EFI system considers historical factors such as age, duration of infertility and previous pregnancies associated with intraoperative findings. The functional score indicates the situation of pelvic organs for a possible future spontane- ous pregnancy. Functional scores are determined by the surgeon and range from 0 to 4 points as follows; absent or nonfunctional as 0, severe dysfunction as 1, moderate dys- function as 2, mild dysfunction as 3, and normal as 4. Not only the minimal functional score, but also other surgical factors such as the rASRM total score and the rASRM endo- metriosis lesion score are included. Finally, the final EFI score is calculated by adding the scores from the history and surgical findings that range from 0 to 10 points, with 10 indicating the best prognosis and 0 the worst prognosis. 2,8 The EFI system has a clear advantage in predicting the outcome of pregnancy and re flects the possible future preg- nancy rate better than the rASRM classi fication, where a score of 6 or more has better RA results than a score of 5 or less. 2,15,16 This classi fication has already been validated externally numerous times and seems to be an interesting tool for patients with endometriosis and infertility. However, the EFI system has the following disadvantages: the classification score does not correlate with pain, as it was not designed for this purpose; as the lowest function score is judged subjectively, the total score may vary by surgeon; it is more complex to use than the rASRM classi fication and the ENZIAN, as it requires the calculation and sum of scores from several categories. 2,8 We believe it is interesting and useful for the group of patients with endometriosis and infertility and for the purpose of calculating probability of a future pregnancy. In 2010, the AAGL initiated a project to develop a new classification of endometriosis. 9 Thirty endometriosis spe- cialists were asked to assign scores ranging from 0 to 10 points, based on the pain, infertility, and surgical dif ficulty of patients with endometriosis. In addition, surgical dif ficulties were categorized into four levels. 9 The visual analogue scale scores and infertility history of patients were collected before surgery for the validation of the scoring system. In 2012, the AAGL Special Interest Group reported that prelim- inary results presented at the AAGL meeting in Las Vegas were encouraging and the AAGL classi fication of endometri- osis was found to be related to pain, infertility, and surgical difficulty. 11 The next step was to conduct a prospective multicenter study with more than 1,500 patients to validate this informa- tion. According to its authors, it still requires adjustments and improvements so that it is globally accepted and applied, as well as further investigations and discussions about this new classification. However, initial evaluations concluded that this classification allows the identi fication of objective intra- operative findings that reliably discriminate the levels of surgical complexity better than the ASRM staging system, and the severity stage correlates with the symptoms of pain and infertility with the ASRM stage. 10 Another interesting data of this classi fication is its easy application in the form of an application with the creation of a final version in pdf, which facilitates storage and a copy for patients (https://apps. apple.com/us/app/aagl-endo-classification/id1592383297 or https://play.google.com/store/apps/details?id¼ br.com.medi- cinia.aagl&hl¼ en&gl ¼ US). AAGL, as one of the largest global Medical Societies in the field of Gynecological Surgery, is putting efforts to test the use of the classi fication even before surgery, by imaging methods. In conclusion, the search for better care for patients with endometriosis is constant given the great implications that this disease brings to physical, social, sexual, reproductive and psychological health. Special attention to its classi fica- tion is needed so we can standardize it globally. In this sense, we believe the classification recently proposed by AAGL may have all the necessary requirements for its wide future use. Conflicts of Interest: None to declare. References 1 Federação Brasileira das Associações de Ginecologia e Obstetrícia. Endometriose. São Paulo: FEBRASGO; 2021. (Protocolo FEBRASGO-Ginecologia, no. 78/Comissão Nacional Especializada em Endometriose) 2 Lee SY, Koo YJ, Lee DH. Classi fication of endometriosis. Yeungnam Univ J Med. 2021;38(01):10 –18. Doi: 10.12701/yujm.2020.00444 Rev Bras Ginecol Obstet Vol. 44 No. 8/2022 © 2022. Federação Bra sileira de Ginecologia e Obste trícia. All rights reserved. Surgical Classification of Endometriosis Nogueira Neto et al.738 3 Dunselman GA, Vermeulen N, Becker C, et al; European Society of Human Reproduction and Embryology. ESHRE guideline: man- agement of women with endometriosis. Hum Reprod. 2014;29 (03):400–412. Doi: 10.1093/humrep/det457 4 Keckstein J, Becker CM, Canis M, et al; Working group of ESGE, ESHRE, and WES. Recommendations for the surgical treatment of endometriosis. Part 2: deep endometriosis. Hum Reprod Open. 2020;2020(01):hoaa002. Doi: 10.1093/hropen/hoaa002 5 Johnson NP, Hummelshoj L, Adamson GD, et al; World Endome- triosis Society Sao Paulo Consortium. World Endometriosis Soci- ety consensus on the classi fication of endometriosis. Hum Reprod. 2017;32(02):315 –324. Doi: 10.1093/humrep/dew293 6 Hornstein MD, Gleason RE, Orav J, et al. The reproducibility of the revised American Fertility Society classi fication of endometriosis. Fertil Steril. 1993;59(05):1015 –1021 7 Tuttlies F, Keckstein J, Ulrich U, et al. [ENZIAN-score, a classi fica- tion of deep in filtrating endometriosis]. Zentralbl Gynäkol. 2005; 127(05):275–281. Doi: 10.1055/s-2005-836904 German. 8 Adamson GD, Pasta DJ. Endometriosis fertility index: the new, validated endometriosis staging system. Fertil Steril. 2010;94 (05):1609–1615. Doi: 10.1016/j.fertnstert.2009.09.035 9 Chapron C, Abrao MS, Miller CE. Endometriosis classi fications need to be revisited: a new one is arriving. NewsScope.. 2012;26 (04):9–10 10 Abrao MS, Andres MP , Miller CE, et al. AAGL 2021 Endometriosis Classification: an anatomy-based surgical complexity score. J Min- im Invasive Gynecol. 2021;28(11):1941 –1950.e1. Doi: 10.1016/j. jmig.2021.09.709 11 Fernando S, Soh PQ, Cooper M, et al. Reliability of visual diagnosis of endometriosis. J Minim Invasive Gynecol. 2013;20(06): 783–789. Doi: 10.1016/j.jmig.2013.04.017 12 Vercellini P, Trespidi L, De Giorgi O, Cortesi I, Parazzini F, Cro- signani PG. Endometriosis and pelvic pain: relation to disease stage and localization. Fertil Steril. 1996;65(02):299 –304 13 Keckstein J, Saridogan E, Ulrich UA, et al. The #Enzian classi fica- tion: A comprehensive non-invasive and surgical description system for endometriosis. Acta Obstet Gynecol Scand. 2021;100 (07):1165–1175. Doi: 10.1111/aogs.14099 14 Montanari E, Dauser B, Keckstein J, Kirchner E, Nemeth Z, Hudelist G. Association between disease extent and pain symptoms in patients with deep in filtrating endometriosis. Reprod Biomed Online. 2019;39(05):845 –851. Doi: 10.1016/j.rbmo.2019.06.006 15 Zeng C, Xu JN, Zhou Y, Zhou YF, Zhu SN, Xue Q. Reproductive performance after surgery for endometriosis: predictive value of the revised American Fertility Society classi fication and the endometriosis fertility index. Gynecol Obstet Invest. 2014;77 (03):180–185. Doi: 10.1159/000358390 16 Wang W, Li R, Fang T, et al. Endometriosis fertility index score maybe more accurate for predicting the outcomes of in vitro fertilisation than r-AFS classi fication in women with endometri- osis. Reprod Biol Endocrinol. 2013;11:112. Doi: 10.1186/1477- 7827-11-112 Rev Bras Ginecol Obstet Vol. 44 No. 8/2022 © 2022. Federação Bras ileira de Ginecologia e Obstetrícia. All rights reserved. Surgical Classification of Endometriosis Nogueira Neto et al. 739